Abstract
Recognizing individuals auditorily is of primal importance in maintaining socio-spatial cohesion among conspecifics within a social group as well as for regulating space use among neighbours, particularly for species dwelling in forests where visual communication is constrained. This study evaluates the capacity of black howler monkeys (Alouatta pigra) in the Palenque National Park, Mexico, to recognize the voices of individual neighbours, using a violation-of-expectation paradigm based on the spatial congruence of voices. First, we assessed intra- vs inter-individual acoustic variations by comparing the acoustic structures of the loud calls of six adult males from three different social groups. Although the acoustic structures of barks were more individually discriminative than those of roars, both loud call types presented significant individual variations. Second, playbacks of sequences composed of barks and roars were studied in order to assess the auditory recognition capacity of six neighbouring groups. Two test situations were presented to each study group: the spatial location of the speaker was either congruent (in the appropriate neighbouring territory) or incongruent (in a territory on the opposite side) with the voice broadcast. Monkeys reacted significantly more (e.g. faster approach, more vocal responses) in incongruent situations. Our data suggest that black howler monkeys display individual acoustic variations and are capable of recognizing the voices of non-group members. Our experimental paradigm is an easily replicable way to investigate inter-group voice recognition in animals and to test the extent of socio-spatial cognitive abilities.


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Altman SA (1959) Field observations on a howling monkey society. J Mammal 40:317–330
Arnold K, Pohlner Y, Zuberbühler K (2008) A forest monkey’s alarm call series to predator models. Behav Ecol Sociobiol 62:549–559
Baldwin JD, Baldwin JI (1976) Vocalizations of howler monkeys (Alouatta palliata) in southwestern Panama. Folia Primatol 26:81–108
Bee MA, Gerhardt HC (2002) Individual voice recognition in a territorial frog (Rana catesbeiana). Proc R Soc Lond B 269:1443–1448
Beer CG (1970) Individual recognition of voice in the social behavior of birds. Adv Stud Behav 3:27–74
Bergman TJ (2010) Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis. Proc R Soc Lond B 277:3045–3053
Boinski S, Mitchell CL (1997) Chuck vocalizations of wild female squirrel monkeys (Saimiri sciureus) contain information on caller identity and foraging activity. Int J Primatol 18:975–993
Bouchet H, Blois-Heulin C, Pellier A-S, Zuberbühler K, Lemasson A (2012) Acoustic variability and individual distinctiveness in the vocal repertoire of red-apped mangabeys (Cercocebus torquatus). J Comp Psychol 126:45–56
Bouchet H, Blois-Heulin C, Lemasson A (2013) Social complexity parallels vocal complexity: a comparison of three non-human primate species. Front Psychol 4:1664–1078
Boyer D, Ramos-Fernández G, Miramontes O, Mateos JL, Cocho G, Larralde H, Rojas F (2006) Scale-free foraging by primates emerges from their interaction with a complex environment. Proc R Soc Lond B 273:1743–1750
Byrne RW (2000) How monkeys find their way: leadership, coordination, and cognitive maps of African baboons. In: Boinski S, Garber PA (eds) On the move: How and Why animals travel in groups. University of Chicago Press, Chicago, pp 491–518
Candiotti A, Zuberbühler K, Lemasson A (2013) Voice discrimination in four primates. Behav Process 99:67–72
Ceugniet M, Izumi A (2004) Vocal individual discrimination in Japanese monkeys. Primates 45:119–128
Chapman CA, Weary DM (1990) Variability in spider monkeys’ vocalizations may provide basis for individual recognition. Am J Primatol 22:279–284
Charrier I, Mathevon N, Jouventin P (2003) Vocal signature recognition of mothers by fur seal pups. Anim Behav 65:543–550
Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367
Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free-ranging vervet monkeys. Am Zool 22:519–529
Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58:67–75
Chivers DJ (1969) On the daily behaviour and spacing of howler monkey groups. Folia Primatol 10:48–102
Crockford C, Boesch C (2003) Context-specific calls in wild chimpanzees, Pan troglodytes verus: analysis of barks. Anim Behav 66:115–125
da Cunha RGT, Byrne RW (2006) Roars of black howler monkeys (Alouatta caraya): evidence for a function in inter-group spacing. Behaviour 143:1169–1199
Dhondt AA, Lambrechts MM (1992) Individual voice recognition in birds. Trends Ecol Evol 7:178–179
Di Fiore A, Campbell CJ (2007) The atelines: variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 155–185
Di Fiore A, Suarez SA (2007) Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications. Anim Cogn 10:317–329
Dunbar RI (1998) The social brain hypothesis. Evol Anthropol 9:178–190
Estrada A, Castellanos L, Ibarra A, García del Valle Y, Muñoz D, Rivera A (2002) Survey of the population of the black howler monkey, Alouatta pigra, at the Mayan site of Palenque, Chiapas, Mexico. Primates 44:51–58
Ey E, Pfefferle D, Fischer J (2007) Do age-and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48:253–267
Fischer JB (1954) Evolution and bird sociality. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a Process, Allen and Unwin, London, pp 71–83
Fischer J (2004) Emergence of individual recognition in young macaques. Anim Behav 67:655–661
Garber PA, Jelinek PE (2006) Travel patterns and spatial mapping in Nicaraguan mantled howler monkeys (Alouatta palliata). In: Rylands AB, Groves CP, Mittermeier RA, Cortés-Ortiz L, Hines JJ (eds) New Perspectives in the Study of Mesoamerican Primates. Springer, New York, pp 287–309
Gautier‐Hion A, Gautier JP (1978) Le singe de Brazza: une strategic originale. Z Tierpsychol 46:84–104
Gouzoules H, Gouzoules S (1990) Matrilineal signatures in the recruitment screams of pigtail macaques, Macaca nemestrina. Behav 327–347
Gunina NA (2011) The role of auditory perception and mental mapping Вестник ТГТУ ISSN 0136–5835. Transactions 17:656-659
Hardouin LA, Tabel P, Bretagnolle V (2006) Neighbour–stranger discrimination in the little owl, Athene noctua. Anim Behav 72:105–112
Hauser MD (1992) Articulatory and social factors influence the acoustic structure of rhesus monkey vocalizations: a learned mode of production. J Acoust Soc Am 91:2175–2179
Herbinger I, Papworth S, Boesch C, Zuberbühler K (2009) Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Anim Behav 78:1389–1396
Janik VM (2000) Whistle matching in wild bottlenose dolphins (Tursiops truncatus). Science 289:1355–1357
Janson CH, Byrne R (2007) What wild primates know about resources: opening up the black box. Anim Cogn 10:357–367
Jordan K, Weiss D, Hauser M, McMurray B (2004) Antiphonal responses to loud contact calls produced by Saguinus oedipus. Int J Primatol 25:465–475
Jorgensen DD, French JA (1998) Individuality but not stability in marmoset long calls. Ethology 104:729–742
Kitchen DM (2000) Aggression and assessment among social groups of Belizean black howler monkeys (Alouatta pigra). Doctoral dissertation, University of Minnesota
Kitchen DM (2004) Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Anim Behav 67:125–139
Kitchen DM (2006) Experimental test of female black howler monkey (Alouatta pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior. Am J Phys Anthropol 131:73–83
Koda H, Lemasson A, Oyakawa C, Pamungkas J, Masataka N (2013) Possible role of mother-daughter vocal interactions on the development of species-specific song in gibbons. PLoS ONE 8:e71432
Kremers D, Lemasson A, Almunia J, Wanker R (2012) Vocal sharing and individual acoustic distinctiveness within a group of captive orcas (Orcinus orca). J Comp Psychol 126:433–445
Lambrechts MM, Dhondt AA (1995) Individual voice discrimination in birds. In: Power DM (ed) Current Ornithology, Vol. 12. Plenum Press, New York, pp 115–139
Lemasson A, Hausberger M (2004) Patterns of vocal sharing and social dynamics in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli). J Comp Psychol 118:347
Lemasson A, Hausberger M (2011) Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). J Acoust Soc Am 129(5):3341–3352
Lemasson A, Palombit RA, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035
Lemasson A, Boutin A, Boivin S, Blois-Heulin C, Hausberger M (2009) Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12:693–704
Lemasson A, Ouattara K, Bouchet H, Zuberbühler K (2010) Speed of call delivery is related to context and caller identity in Campbell’s monkey males. Naturwissenschaften 97:1023–1027
Lemasson A, Mikus MA, Blois-Heulin C, Lodé T (2013) Social partner discrimination based on sounds and scents in Asian small-clawed otters (Aonyx cinereus). Naturwissenschaften 100:1–5
Levréro F, Durand L, Vignal C, Blanc A, Mathevon N (2009) Begging calls support offspring individual identity and recognition by zebra finch parents. Comptes rendus biologies 332:579–589
Levréro F, Mathevon N (2013) Vocal signature in wild infant chimpanzees. Am J Primatol 75:324–332
Lührs ML, Dammhahn M, Kappeler PM, Fichtel C (2009) Spatial memory in the grey mouse lemur (Microcebus murinus). Anim Cogn 12:599–609
Marler P (1967) Animal communication signals. Science 157:769–774
Marler P, Hobbett L (1975) Individuality in a long-range vocalization of wild chimpanzees. Z Tierpsychol 38:97–109
McComb K, Reby D, Baker L, Moss C, Sayialel S (2003) Long-distance communication of acoustic cues to social identity in African elephants. Anim Behav 65:317–329
Mitani JC (1985) Responses of gibbons (Hylobates muelleri) to self, neighbor, and stranger song duets. Int J Primatol 6:193–200
Mitani JC, Gros-Louis J, Macedonia JM (1996) Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. Int J Primatol 17:569–583
Noë R, Laporte M (2014) Socio-spatial cognition in vervet monkeys. Anim Cogn 17:597–607
Noser R, Byrne RW (2007) Mental maps in chacma baboons (Papio ursinus): using inter-group encounters as a natural experiment. Anim Cogn 10:331–340
Oliveira DAG, Ades C (2002) Long-distance calls in neotropical primates. An Acad Brasil Ci 76:393–398
Owren MJ, Rendall D (2001) Sound on the rebound: bringing form and function back to the forefront in understanding non-human primate vocal signaling. Evol Anthropol: Issues News Rev 10:58–71
Oyakawa C, Koda H, Sugiura H (2007) Acoustic features contributing to the individuality of wild agile gibbon (Hylobates agilis agilis) songs. Am J Primatol 69:777–790
Proops L, McComb K, Reby D (2009) Cross-modal recognition in domestic horses (Equus caballus). Proc Natl Acad Sci U S A 106:947–951
Raichel DR (2006) The science and applications of acoustics. Springer, Colorado
Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015
Rendall D, Owren MJ, Rodman PS (1998) The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. J Acoust Soc Am 103:602–614
Rendall D, Cheney DL, Seyfarth RM (2000) Proximate factors mediating ‘contact’ calls in adult female baboons and their infants. J Comp Psychol 114:36–46
Rendall D, Notman H, Owren MJ (2009) Asymmetries in the individual distinctiveness and maternal recognition of infant contact calls and distress screams in baboons. J Acoust Soc Am 125:1792–1805
Sankey C, Henry S, André N, Richard-Yris MA, Hausberger M (2011) Do horses have a concept of person? PLoS ONE 6:e18331
Sekulic R (1982) The function of howling in red howler monkeys (Alouatta seniculus). Behaviour 81:39–54
Sekulic R (1983) The effect of female call on male howling in red howler monkeys (Alouatta seniculus). Int J Primatol 4:291–305
Seyfarth RM, Cheney DL (2009) Seeing who we hear and hearing who we see. Proc Natl Acad Sci U S A 106:669–670
Snowdon CT, Cleveland J (1980) Individual recognition of contact calls by pygmy marmosets. Anim Behav 28:717–727
Steenbeek R, Assink P (1998) Individual differences in long-distance calls of male wild Thomas langurs (Presbytis thomasi). Folia Primatol 69:77–80
Teixidor P, Byrne RW (1997) Can spider monkeys (Ateles geoffroyi) discriminate vocalizations of familiar individuals and strangers?. Folia Primatol 68:254–264
Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537
Townsend SW, Allen C, Manser MB (2012) A simple test of vocal individual recognition in wild meerkats. Biol Lett 8:179–182
Treves A, Drescher A, Ingrisano N (2001) Vigilance and aggregation in black howler monkeys (Alouatta pigra). Behav Ecol Sociobiol 50:90–95
Tripovich JS, Charrier I, Rogers TL, Canfield R, Arnould JP (2008) Acoustic features involved in the neighbour–stranger vocal recognition process in male Australian fur seals. Behav Process 79:74–80
Trivers RL (1971) Evolution of reciprocal altruism. Q Rev Biol 46:35–57
Van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A, Garber AP, Mary Pavelka SMM, LeAndra L (eds) New perspectives in the study of Mesoamerican primates, 4th edn. Springer, New York, pp 121–142
Van Belle S, Estrada A, Strier KB (2008) Social relationships among male Alouatta pigra. Int J Primatol 29:1481–1498
Van Belle S, Estrada A, Ziegler TE, Strier KB (2009) Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. Am J Primatol 71:153–164
Van Belle S, Estrada A, Strier KB, Di Fiore A (2012) Genetic structure and kinship patterns in a population of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Am J Primatol 74:948–957
Van Belle S, Estrada A, Garber PA (2013) Spatial and diurnal distribution of loud calling in black howlers (Alouatta pigra). Int J Primatol 34:1209–1224
Waser PM (1977) Individual recognition, intragroup cohesion, and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74
Whitehead JM (1985) Long-distance vocalizations and spacing in mantled howling monkeys, Alouatta palliata. Doctoral dissertation, University of North Carolina at Chapel Hill
Whitehead J (1995) Vox Alouattinae: a preliminary survey of the acoustic characteristics of long-distance calls of howling monkeys. Int J Primatol 16:121–144
Wich SA, Assink PR, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): the effect of familiarity. Behaviour 139:79–88
Xitco MJ, Gory JD, Kuczaj SA (2004) Dolphin pointing is linked to the attention behaviour of a receiver. Anim Cogn 7:231–238
Ydenberg RC, Giraldeau LA, Falls JB (1988) Neighbours, strangers, and the asymmetric war of attrition. Anim Behav 36:343–347
Zimmermann E, Lerch C (1993) The complex acoustic design of an advertisement call in male mouse lemurs (Microcebus murinus, Prosimii, Primates) and sources of its variation. Ethology 93:211–224
Zuberbühler K, Wittig RM (2011) Field experiments with non-human primates: a tutorial. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology: A practical guide, 2nd edn. Cambridge University Press, Cambridge, pp 207–224
Acknowledgments
We are very grateful to the Mexican government (CONANP) for the authorization to carry out our research at the Palenque National Park. Our research was supported by grants from CONACyT, the graduate program in biological sciences (UNAM), CNRS (PICS program), ANR, IUF and IDEA WILD. We are grateful to The Institute of Biology (UNAM) and Animal and Human Ethology Laboratory (University of Rennes 1) staff members for logistic support. We thank Eloise Chailleux, Cindy Maslarova and Oskar Persson for their assistance in the field. We are grateful to Dr. Sarie Van Belle for her helpful comments and for her assistance with the identification of monkeys. We are also grateful to Ernesto Estivill and to Veronique Biquand for their assistance in acoustic and statistic and to Ann Cloarec and Anne-Marie Cervera for correcting our English. We would like to thank the anonymous reviewers for their helpful comments. This article is a partial requirement for the doctoral degree in biological sciences at the National Autonomous University of Mexico (UNAM) by MBJ.
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Experiments comply with the current laws of Mexico.
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Briseño-Jaramillo, M., Estrada, A. & Lemasson, A. Individual voice recognition and an auditory map of neighbours in free-ranging black howler monkeys (Alouatta pigra). Behav Ecol Sociobiol 69, 13–25 (2015). https://doi.org/10.1007/s00265-014-1813-9
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DOI: https://doi.org/10.1007/s00265-014-1813-9

